The systematic significance of floral morphology,nectaries, and nectar concentration in epiphytic cacti of tribes Hylocereeae and Rhipsalideae (Cactaceae)

A long-standing interest in cactus taxonomy has existed since the Linnaean generation, but an appreciation of the reproductive biology of cacti started early in the 1900s. Numerous studies indicate that plant reproductive traits provide valuable systematic information. Despite the extensive reproductive versatility and specializations in breeding systems coupled with the striking floral shapes, the reproductive biology of the Cactaceae has been investigated in approximately 10% of its species. Hence, the systematic value of architectural design and organization of internal floral parts has remained virtually unexplored in the family. This study represents the most extensive survey of flower and nectary morphology in the Cactaceae focusing on tribes Hylocereeae and Rhipsalideae (subfamily Cactoideae). Our objectives were (1) to conduct comparative morphological analyses of flowers and floral nectaries and (2) to compare nectar solute concentration in these two tribes consisting of holo- and semi-epiphytic species. Flower morphology, nectary types, and sugar concentration of nectar have strong taxonomic implications at the tribal, generic and specific levels. Foremost, three types of nectaries were found, namely chamber nectary (with the open and diffuse subtypes), furrow nectary (including the holder nectary subtype), and annular nectary. All Hylocereeae species possess chamber nectaries, in which the nectarial tissue has both trichomes and stomata. The Rhipsalideae are distinguished by two kinds of floral nectaries: furrow and annular, both nectary types with stomata only. The annular nectary type characterizes the genus Rhipsalis. Nectar concentration is another significant taxonomic indicator separating the Hylocereeae and Rhipsalideae and establishing trends linked to nectar sugar concentration and amount of nectar production in relation to flower size. There is an inverse relationship between flower size and amount of nectar production in the smaller Rhipsalideae flowers, in which nectar concentration is more than two-fold higher despite the smaller volume of nectar produced when compared to the large Hylocereeae flowers. Variability of nectary morphology and nectar concentration was also evaluated as potential synapomorphic characters in recent phylogenies of these tribes. In conclusion, our data provide strong evidence of the systematic value of floral nectaries and nectar sugar concentration in the Cactaceae, particularly at different taxonomic levels in the Hylocereeae and Rhipsalideae.     

Influence of elevated CO2 and ultraviolet-B radiation levels on floral nectar production: a nectary-morphological perspective

 Investigations of the effects of two global events – elevated CO₂ levels and enhanced ultraviolet-B (UV-B) radiation – on floral nectar production are reviewed from twelve dicotyledonous families. Furthermore, to allow comparisons between nectary morphology and nectar production in treated plants of these fifteen species, new data on floral nectary structure are provided for Malcolmia maritima (L.) R. Br. (Brassicaceae) and Scabiosa columbaria L. (Dipsacaceae). All but the last taxon possessed mesenchymatic floral nectaries with surface stomata. Few clear relationships existed between nectary morphology and various physiological responses to CO₂ or UV-B enrichment, indicating that species responded notwithstanding nectary structure itself. Overall, nectar-solute concentration was least affected by elevated CO₂ or UV-B radiation; consequently, changes in nectar volume were responsible for differences in nectar-sugar production per flower. Three species of Fabaceae experienced no change in floral nectar production upon exposure to elevated CO₂. To date, no study of enhanced UV-B radiation reported a consistent reduction in floral nectar production; three species of Brassicaceae responded differently, but various levels of ozone depletion were simulated. Experimentation with more taxa – including those possessing nectary types such as septal (gynopleural) nectaries (e.g. many monocotyledons) or aggregations of glandular trichomes – and expanding such physiological studies to species possessing extrafloral nectaries, are recommended. Received August 8, 2002; accepted November 23, 2002 Published online: June 2, 2003     

Catching ants with honey: an experimental test of distraction and satiation as alternative modes of escape from flower-damaging ants

According to the distraction hypothesis, extrafloral nectaries (EFN) evolved under selection to entice ants away from floral nectaries, reducing ant-mediated damage to flowers and/or interference with pollinators. Predator-satiation, through production of nectar in either surplus flowers or EFN, provides an alternative mechanism for reducing the impact of ants as flower visitors. I tested these two hypotheses by experimentally adding EFN to flowering plants of the alpine wildflower, Polemonium viscosum, and by surveying the relationship between ant visitation and nectary number in nature. Plants of P. viscosum lack EFN and experience flower damage by ants of Formica neorufibarbus gelida. Ant behavior was compared on plants with five flowers and three experimental EFN and on controls with equal floral display, but no EFN. Addition of EFN increased flower visitation by ants. The effect of EFN on flower visitation did not depend on proximity of EFN to flowers or attractiveness of EFN to ants. Findings suggest that ants perceived patch quality on a whole plant basis, rather than responding to EFN and flowers as distinct nectar patches. Ant visitation did not keep pace with nectary number in nature. The relationship between ant visitation and nectary number per plant was weak and shallow as predicted under satiation. Ant foraging choices on experimental inflorescences showed that ants bypass flowers avoided by earlier ants, enhancing probability of escape via satiation. Results do not support the idea that EFN evolve to reduce flower visitation by ants, but show instead that nectar in surplus flowers can satiate ants and reduce their negative impacts on flower function and integrity.     

长药景天花蜜腺的发育解剖学研究

长药景天花蜜腺５枚,呈侧向扁平的舌形或弯月形,分别位于５株离生心皮的外侧,两者的基部相连,属于子房蜜腺。蜜腺由分泌表皮、产蜜组织和仅含韧皮部的维管束组成。长药景天花蜜腺起源于心皮外侧基部的表层结构。产蜜组织在发育过程中,细胞中的液泡体积及淀粉粒呈现有规律的消长变化。泌蜜后期,蜜腺组织从上往下液泡化,具明显的方向性。根据其结构及多糖变化分析,来自韧皮部的原蜜汁以淀粉粒形式贮存于产蜜组织中,泌蜜期水解     

垂柳花蜜腺的发育解剖学研究

垂柳雌花蜜腺一枚,位于于房与花序轴之间,多呈扁平广卵形,由分泌表皮、泌蜜组织和维管束组成。雄花蜜腺呈基部相连的两枚突起,一枚位于花丝与花序轴之间,基部宽扁,上部棒状;另一枚位于花丝与苞片之间,棒状,仅由分泌表皮和泌蜜组织组成。雌、雄花蜜腺均起源于花托表面2—3层细胞。在蜜腺发育过程中,雌、雄花蜜腺泌蜜组织细胞的液泡发生规律性变化．雌花蜜腺为淀粉型蜜腺,而雄花蜜腺为非淀粉型蜜腺。雌、雄花蜜腺的原宜汁分别由蜜腺维管束韧应部或花丝维管束韧皮部提供,其蜜计最后均由分泌表皮细胞和变态气孔排出。     

Nectary structure and nectar presentation in Aloe castanea and A. greatheadii var. davyana (Asphodelaceae)

This paper deals with the nectary structure and nectar presentation of two species belonging to different sections of the genus Aloe: A. castanea (Anguialoe) and A. greatheadii var. davyana (Pictae). The development of the nectary was studied by means of bright field and fluorescence light microscopy and scanning electron microscopy (SEM) in three flower stages (young, intermediate, old). Both species have septal nectaries. In A. castanea, a subsidiary tissue, not present in A. greatheadii var. davyana, was found beneath the nectary epithelium. This tissue accumulated starch that was hydrolyzed during secretion. Starch was slightly accumulated around the nectary in A. greatheadii var. davyana. The distribution of chlorophyll in the ovary was also different in the two species. These anatomical differences are not, however, correlated with greater nectar production in A. castanea. In this species, the nectary seems to degenerate after secretion, while in A. greatheadii var. davyana no sign of degeneration was observed. Differences in nectar presentation among the two species may account for different pollinators visiting their flowers.     

Nectary structure of Labiatae in relation to their nectar secretion and characteristics in a Mediterranean shrub community — Does flowering time matter?

We studied the interrelation between nectary structure (13 parameters), nectar characteristics (yield, chemical composition), and flower size of 11 Labiatae species in a Mediterranean shrub community near Athens, Greece. We also explored whether the above attributes are affected by the Mediterranean summer drought constraints. Our findings show that among all nectary parameters studied, nectary size and stomatal opening are the most important in (positively) shaping nectar secretion, nectary size being the most meaningful. Nectary structure is correlated to quantity of the nectar secreted, not its quality. Wide flowers bear wide nectaries with large stomatal openings, whereas deep flowers are not related to any nectary size. Corolla size (both length and width) and nectary stomatal opening decrease with flowering time. This applies also to nectary size, nectar volume and sugar content of the perennials (9 species). All above cases of time dependence show that there is a constraint effect of Mediterranean climate on floral and nectary structure, reflected also as a decrease in nectar secretion. Nectary structure in Labiatae is largely shaped by both phylogenetic and climate constraints. On the other hand, although nectar is largely influenced by nectary structure, it is to a large extent ecologically biased, implying that, in addition to phylogeny, there are many other ecological parameters interfering in its secretion such as time within the season, life history, and light requirements.     

Occurrence,structure, ontogeny and biology of nectaries inKigelia pinnata DC

The occurrence, morphology, ontogeny, structure and preliminary nectar analysis of floral and extrafloral nectaries are studied inKigelia pinnata of the Bignoniaceae. The extrafloral nectaries occur on foliage leaves, sepals and outer wall of the ovary, while the floral nectary is situated around the ovary base as an annular, massive, yellowish ring on the torus. The extrafloral nectaries originate from a single nectary initial. The floral nectary develops from a group of parenchymatous cells on the torus. The extrafloral nectaries are differentiated into multicellular foot, stalk and cupular or patelliform head. The floral nectary consists of parenchymatous tissue. The floral nectaries are supplied with phloem tissue. The secretion is copious in floral nectary. Function of the nectary, preliminary nectar analysis, and symbiotic relation between nectaries and animal visitors are discussed.     

Anatomical and ultrastructural changes of the floral nectary ofPisum sativum L. during flower development

Summary The floral nectary ofPisum sativum L. is situated on the receptacle at the base of the gynoecium. The gland receives phloem alone which departed the vascular bundles supplying the staminal column. Throughout the nectary, only the companion cells of the phloem exhibited wall ingrowths typical of transfer cells. Modified stomata on the nectary surface served as exits for nectar, but stomatal pores developed well before the commencement of secretion. Furthermore, stomatal pores on the nectary usually closed by occlusion, not by guard-cell movements. Pore occlusion was detected most frequently in post-secretory and secretory glands, and less commonly in pre-secretory nectaries. A quantitative stereological study revealed few changes in nectary fine structure between buds, flowers secreting nectar, and post-secretory flowers. Dissolution of abundant starch grains in plastids of subepidermal secretory cells when secretion commenced suggests that starch is a precursor of nectar carbohydrate production. Throughout nectary development, mitochondria were consistently the most plentiful organelle in both epidermal and subepidermal cells, and in addition to the relative paucity of dictyosomes, endoplasmic reticulum, and their associated vesicles, the evidence suggests that floral nectar secretion inP. sativum is an energy-requiring (eccrine) process, rather that granulocrine.Abbreviations ER endoplasmic reticulum - GA glutaraldehyde - SEM scanning electron microscopy     

Nectar biodiversity: a short review

 Nectaries differ in many aspects but a common feature is some kind of advantage for the plant conferred by foraging of consumers which may defend the plant from predators in the case of extrafloral nectaries, or be agents of pollination in the case of floral nectaries. This minireview is concerned mainly with floral nectaries and examines the following characteristics: position in flower; nectary structure; origin of carbohydrates, aminoacids and proteins; manner of exposure of nectar; site of nectar presentation; volume and production of nectar in time; sexual expression of flower and nectary morphology; nectar composition and floral sexual expression; variability of nectar composition; fate of nectar; energy cost of nectar production. The species of certain large families, such as Brassicaceae, Lamiaceae and Asteraceae, resemble each other in nectary organisation; other families, such as Cucurbitaceae and Ranunculaceae, have various types of organisation. A scheme is presented to illustrate factors influencing nectary and nectar biodiversity. Received July 23, 2002; accepted September 18, 2002 Published online: June 2, 2003     

Is nectar reabsorption restricted by the stalk cells of floral and extrafloral nectary trichomes?

Reabsorption is a phase of nectar dynamics that occurs concurrently with secretion; it has been described in floral nectaries that exude nectar through stomata or unicellular trichomes, but has not yet been recorded in extrafloral glands. Apparently, nectar reabsorption does not occur in multicellular secretory trichomes (MST) due to the presence of lipophilic impregnations – which resemble Casparian strips – in the anticlinal walls of the stalk cells. It has been assumed that these impregnations restrict solute movement within MST to occur unidirectionally and exclusively by the symplast, thereby preventing nectar reflux toward the underlying nectary tissues. We hypothesised that reabsorption is absent in nectaries possessing MST. The fluorochrome lucifer yellow (LYCH) was applied to standing nectar of two floral and extrafloral glands of distantly related species, and then emission spectra from nectary sections were systematically analysed using confocal microscopy. Passive uptake of LYCH via the stalk cells to the nectary tissues occurred in all MST examined. Moreover, we present evidence of nectar reabsorption in extrafloral nectaries, demonstrating that LYCH passed the stalk cells of MST, although it did not reach the deepest nectary tissues. Identical (control) experiments performed with neutral red (NR) demonstrated no uptake of this stain by actively secreting MST, whereas diffusion of NR did occur in plasmolysed MST of floral nectaries at the post‐secretory phase, indicating that nectar reabsorption by MST is governed by stalk cell physiology. Interestingly, non‐secretory trichomes failed to reabsorb nectar. The role of various nectary components is discussed in relation to the control of nectar reabsorption by secretory trichomes.     

荆条花蜜腺发育解剖学研究

荆条（Ｖｉｔｅｘ ｃｈｉｎｅｎｓｉｓ Ｍｉｌｌ．）花蜜腺属于淀粉型子房蜜腺,呈圆筒状环绕于子房的基部。蜜腺外观上无特殊结构,表面有。由分泌表皮和泌蜜组织组成,包括分泌表皮、气孔器、泌蜜薄壁组织和维管束。密腺和子房壁起源相同。花蕾膨大期,泌蜜组织细胞中产生大液泡;露冠期,泌蜜组织中形成维管束;花蕾初放期,分泌表皮细胞分化形成气孔器,无气孔下室,淀粉粒的积累在此期达到高峰;盛花期,蜜腺中已无淀粉粒,密     

Nectaries and reproductive biology of Croton sarcopetalus (Euphorbiaceae)

Flower morphology, nectary structure, nectar chemical composition, breeding system, floral visitors and pollination were analysed in Croton sarcopetalus , a diclinous-monoecious shrub from Argentina. Male flowers have five receptacular nectaries, with no special vascular bundles, that consist of a uniserial epidermis with stomata subtended by a secretory parenchyma. Female flowers bear two different types of nectaries: inner (IN) and outer (ON) floral nectaries. IN, five in all, are structurally similar to the nectaries of male flowers. The five ON are vascularized, stalked, and composed of secretory, column-shaped epidermal cells without stomata subtended by secretory and ground parenchyma. In addition, ON act as post-floral nectaries secreting nectar during fruit ripening. Extrafloral nectaries (EFN) are located on petioles, stipules and leaf margins. Petiolar EFN are patelliform, stalked and anatomically similar to the ON of the female flower. Nectar sampled from all nectary types is hexose dominant, except for the ON of the female flower at the post-floral stage that is sucrose dominant. The species is self-compatible, but geitonogamous fertilization is rarely possible because male and female flowers are not usually open at the same time in the same individual, i.e. there is temporal dioecism. Flowers are visited by 22 insect species, wasps being the most important group of pollinators. No significant differences were found in fruit and seed set between natural and hand pollinated flowers. This pattern indicates that fruit production in this species is not pollen/pollinator limited and is mediated by a wide array of pollinators.     

Comparative anatomy and morphology of nectar-producing Melastomataceae

Background and Aims

Most neotropical Melastomataceae have bee-pollinated flowers with poricidal anthers. However, nectar rewards are known to be produced in about 80 species in eight genera from four different tribes. These nectar-producing species are pollinated by both vertebrates and invertebrates.

Methods

The floral morphology and anatomy of 14 species was studied in six genera of nectar-producing Melastomataceae (Blakea, Brachyotum, Charianthus, Huilaea, Meriania and Miconia). Anatomical methods included scanning electron microscopy, and serial sections of paraffin-embedded flowers.

Key Results

All vertebrate-pollinated melastome flowers have petals that do not open completely at anthesis, thus forming a pseudo-tubular corolla, while closely related species that are bee pollinated have rotate or reflexed corollas. In most species, nectar secretion is related to stomatal or epidermal nectaries and not filament slits as previously reported. Moreover, the nectar is probably supplied by large vascular bundles near the release area. Blakea and Huilaea have nectary stomata located upon the dorsal anther connective appendages. Brachyotum also has nectary stomata on the anther connectives, but these are distributed lengthwise along most of the connective. Meriania may release nectar through the anther connective, but has additional nectary stomata on the inner walls of the hypanthium. Miconia has nectary stomata on the ovary apex. Charianthus nectaries were not found, but there is circumstantial evidence that nectar release occurs through the epidermis at the apex of the ovary and the lower portions of the inner wall of the hypanthium.

Conclusions

Nectar release in Melastomataceae is apparently related to nectary stomata and not filament slits. The presence of nectary stomata on stamens and on ovary apices in different lineages suggests that the acquisition of nectaries is a derived condition. Nectary location also supports a derived condition, because location is strongly consistent within each genus, but differs between genera.Key words: Blakea, Brachyotum, Charianthus, Huilaea, Meriania, Melastomataceae, Miconia, nectaries, nectary stomata, pollination     

芝麻菜花蜜腺的结构和发育研究

通过解剖镜观察、石蜡切片和薄切片等方法,对芝麻菜的花蜜腺的位置、形态、结构、发育过程及泌蜜前后组织化学变化进行了研究。芝麻菜花蜜腺4枚,分成两对,其中一对侧蜜腺较大,棱柱状,分别着生在外轮2个短雄蕊基部内侧的花托上,结构上由表皮、产蜜组织和维管组织构成;另一对中蜜腺较小,近棒状,分别着生在内轮4个长雄蕊外侧的花托上,结构上仅由表皮和产蜜组织构成。二者表皮细胞外都具角质层,且蜜腺产蜜组织细胞中只含少量的多糖物质。两类蜜腺的蜜汁均由变态气孔泌出体外。无论侧蜜腺还是中蜜腺,蜜腺原基皆是在雌、雄蕊已分化后,由花托相应位置表皮下的1～2层细胞分裂形成的。在蜜腺发育中,产蜜组织细胞在泌蜜前后不具明显的液泡变化。     

The evolution of floral nectaries in Disa (Orchidaceae: Disinae): recapitulation or diversifying innovation?

Background and Aims

The Orchidaceae have a history of recurring convergent evolution in floral function as nectar production has evolved repeatedly from an ancestral nectarless state. However, orchids exhibit considerable diversity in nectary type, position and morphology, indicating that this convergence arose from alternative adaptive solutions. Using the genus Disa, this study asks whether repeated evolution of floral nectaries involved recapitulation of the same nectary type or diversifying innovation. Epidermis morphology of closely related nectar-producing and nectarless species is also compared in order to identify histological changes that accompanied the gain or loss of nectar production.

Methods

The micromorphology of nectaries and positionally equivalent tissues in nectarless species was examined with light and scanning electron microscopy. This information was subjected to phylogenetic analyses to reconstruct nectary evolution and compare characteristics of nectar-producing and nectarless species.

Key Results

Two nectary types evolved in Disa. Nectar exudation by modified stomata in floral spurs evolved twice, whereas exudation by a secretory epidermis evolved six times in different perianth segments. The spur epidermis of nectarless species exhibited considerable micromorphological variation, including strongly textured surfaces and non-secreting stomata in some species. Epidermis morphology of nectar-producing species did not differ consistently from that of rewardless species at the magnifications used in this study, suggesting that transitions from rewardlessness to nectar production are not necessarily accompanied by visible morphological changes but only require sub-cellular modification.

Conclusions

Independent nectary evolution in Disa involved both repeated recapitulation of secretory epidermis, which is present in the sister genus Brownleea, and innovation of stomatal nectaries. These contrasting nectary types and positional diversity within types imply weak genetic, developmental or physiological constraints in ancestral, nectarless Disa. Such functional convergence generated by morphologically diverse solutions probably also underlies the extensive diversity of nectary types and positions in the Orchidaceae.     

Floral ontogeny of Cneorum tricoccon L. (Rutaceae)

The floral ontogeny of the Spurge olive (Cneorum tricoccon L.) is studied by means of scanning electron microscopic observations. Special attention is paid to the sequence of initiation of the floral parts, the occurrence of septal cavities, and the development of the nectariferous tissue. The nectary disc arises as a receptacular outgrowth below the ovary and independently from stamen development. By the extensive growth of this voluminous androgynophore, stamen filaments become enclosed by nectary tissue and as a result, they are seated in pits between the lobes of the disc. Between ovary and style, three lobes are present, which are covered with stomata – their function is unknown. The significance of the unusual trimery of the flower is discussed. Floral developmental evidence supports a Rutalean affinity, although more ontogenetic investigations are needed in Rutaceae, subfamily Spathelioideae.     

Floral nectar production and carbohydrate composition and the structure of receptacular nectaries in the invasive plant <Emphasis Type="Italic">Bunias orientalis</Emphasis> L. (Brassicaceae)

The data relating to the nectaries and nectar secretion in invasive Brassicacean taxa are scarce. In the present paper, the nectar production and nectar carbohydrate composition as well as the morphology, anatomy and ultrastructure of the floral nectaries in Bunias orientalis were investigated. Nectary glands were examined using light, fluorescence, scanning electron and transmission electron microscopy. The quantities of nectar produced by flowers and total sugar mass in nectar were relatively low. Total nectar carbohydrate production per 10 flowers averaged 0.3 mg. Nectar contained exclusively glucose (G) and fructose (F) with overall G/F ratio greater than 1. The flowers of B. orientalis have four nectaries placed at the base of the ovary. The nectarium is intermediate between two nectary types: the lateral and median nectary type (lateral and median glands stay separated) and the annular nectary type (both nectaries are united into one). Both pairs of glands represent photosynthetic type and consist of epidermis and glandular tissue. However, they differ in their shape, size, secretory activity, dimensions of epidermal and parenchyma cells, thickness of secretory parenchyma, phloem supply, presence of modified stomata and cuticle ornamentation. The cells of nectaries contain dense cytoplasm, plastids with starch grains and numerous mitochondria. Companion cells of phloem lack cell wall ingrowths. The ultrastructure of secretory cells indicates an eccrine mechanism of secretion. Nectar is exuded throughout modified stomata.     

The floral nectaries in theLimnanthaceae

Floral nectaries in theLimnanthaceae are established as exoscopic basal bulges of the episepalous stamens. Their nectariferous tissues include the epidermis and hypodermal parenchyma and inLimnanthes are vascularized by phloematic branches of the staminal bundles. Secretion occurs mainly through anomocytic stomata but, in addition, probably through the outer cuticularized thin walls of the epidermal cells. The flower structure is comparatively simple. The nectar is often slightly concealed. A wide range of pollinators can be expected, but bees are observed to be the dominant ones. The systematic position of the family is still obscure. Taxonomic placement near to any other geranialian families or to theCaryophyllaceae is only weakly justified.The floral nectaries of theGeraniales and their systematic implications II. For the first part seeLink (1992).